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The Origins of Multicellularity and the Early History of the Genetic Toolkit

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The Origins of Multicellularity and the Early History of the Genetic Toolkit ANRV361-GE42-11 ARI 1 October 2008 20:20 ANNUAL The Origins of REVIEWS Further Click here for quick links to Annual Reviews content online, Multicellularity and the Early including: • Other articles in this volume • Top cited articles History of the Genetic Toolkit • Top downloaded articles • Our comprehensive search For Animal Development Antonis Rokas Vanderbilt University, Department of Biological Sciences, Nashville, Tennessee 37235; email: [email protected] Annu. Rev. Genet. 2008. 42:235–51 Key Words The Annual Review of Genetics is online at cell adhesion, cell-cell signaling, transcriptional regulation, animal genet.annualreviews.org phylogeny, choanoflagellate, repeated evolution This article’s doi: 10.1146/annurev.genet.42.110807.091513 Abstract Copyright c 2008 by Annual Reviews. Multicellularity appeared early and repeatedly in life’shistory; its instan- All rights reserved tiations presumably required the confluence of environmental, ecolog- 0066-4197/08/1201-0235$20.00 ical, and genetic factors. Comparisons of several independently evolved pairs of multicellular and unicellular relatives indicate that transitions to multicellularity are typically associated with increases in the numbers of genes involved in cell differentiation, cell-cell communication, and Annu. Rev. Genet. 2008.42:235-251. Downloaded from www.annualreviews.org Access provided by Houston Baptist University on 02/03/20. For personal use only. adhesion. Further examination of the DNA record suggests that these increases in gene complexity are the product of evolutionary innova- tion, tinkering, and expansion of genetic material. Arguably, the most decisive multicellular transition was the emergence of animals. Decades of developmental work have demarcated the genetic toolkit for animal multicellularity, a select set of a few hundred genes from a few dozen gene families involved in adhesion, communication, and differentiation. Examination of the DNA records of the earliest-branching animal phyla and their closest protist relatives has begun to shed light on the origins and assembly of this toolkit. Emerging data favor a model of gradual as- sembly, with components originating and diversifying at different time points prior to or shortly after the origin of animals. 235 ANRV361-GE42-11 ARI 1 October 2008 20:20 INTRODUCTION specific genes (83), and the elaborate coordi- nation of developmental processes, made them From the simple, undifferentiated bacterial fil- stand out as one of the most complex inventions Complexity: a aments to the macroscopic multicellular forms of multicellularity (7, 19, 46, 70). Elucidating problematic term used seen in animals, plants, and fungi, the 25 or the enigma of the origins of multicellularity in in a variety of different so instantiations of multicellularity extant to- contexts; here it is used animals requires, to a large extent, solving the day exhibit a remarkable diversity in genotypic to simply denote enigma of the origins of their development. and phenotypic complexity (5, 51) (Table 1). increases in numbers But what is the genetic basis of animal multi- of cell types, body size, For example, the multicellular forms observed cellularity and development? Animal genomes life-cycle stages, genes, in prokaryotes are architecturally and morpho- contain thousands of genes involved in carrying or protein domains logically relatively simple, characterized by the out vital routine tasks, such as metabolism and presence, at their most elaborate manifesta- cell division. Many of these genes are shared tions, of a few distinct cell types (9). Similar lev- across eukaryotes and predate the origin of ani- els of complexity are observed in most cases of mals per se (23, 60), but some underwent exten- eukaryotic multicellularity (7, 9, 103). The in- sive gene duplications and evolved new roles in dependent transitions to multicellularity from the construction and patterning of animal bod- unrelated unicellular ancestors offer a unique ies. These genes comprise the genetic toolkit opportunity for comparative study, especially at for animal development (20, 57), a select set the molecular level. We start by identifying the of a few hundred genes from a few dozen gene general conditions favoring the emergence of families involved in three key processes: cell dif- multicellularity, its origins, and its signature in ferentiation, cell-cell communication, and cell the DNA record. adhesion. Examples of toolkit components in- Most multicellular lineages are charac- clude the Hox transcription factors (35), the cell terized by relatively simple architectures and signaling families of Wnts and receptor tyrosine morphologies. However, on a few separate kinases (53, 62), as well as the gene families of occasions, the transition to multicellularity has cadherins and integrins, which are involved in burgeoned into macroscopic, architecturally cell adhesion (1, 72). Understanding the origins complex body plans (e.g., plants, fungi, and ani- and assembly of the genetic toolkit required for mals) (9). In animals, for example, the evolution animal multicellularity and development is the of several differentiated cell types generated by second and central focus of this review. the specific expression of a number of cell-type– Table 1 The genetic and phenotypic complexity of select, independently evolved, multicellular bacterial and eukaryotic lineages Representative Annu. Rev. Genet. 2008.42:235-251. Downloaded from www.annualreviews.org 1 Access provided by Houston Baptist University on 02/03/20. For personal use only. Lineage Cell type number species Gene number Genome size (Mb) References Actinobacteria 3 Streptomyces coelicolor 7825 9 (8) Cyanobacteria 3 Nostoc punctiforme 7432 9 (69) Myxobacteria 3 Myxococcus xanthus 7388 9 (14, 38) Cellular slime molds 3 Dictyostelium discoideum 13,541 34 (7, 32) Animals 3–122 Drosophila melanogaster 13,733 200 (7, 24) Fungi 3–9 Coprinus cinereus2 13,544 37.5 (7) Volvocine green algae 2 Volvox carteri3 15,544 140 (7) Plants 5–44 Arabidopsis thaliana 25,498 125 (24, 100) 1The first three lineages are bacterial; the rest eukaryotic. 2Genome unpublished; data retrieved from the Broad Institute (http://www.broad.mit.edu/). 3Genome unpublished; data retrieved from the Joint Genome Institute (http://www.jgi.doe.gov/). 236 Rokas ANRV361-GE42-11 ARI 1 October 2008 20:20 Insights from paleontology, ecology, and multicellular setting by functional specializa- phylogenetics provide the temporal, environ- tion, at least in principle. mental, and historical context within which we In several instances, theoretical expectations Myxobacteria: a can understand the emergence of multicellu- have been put to the test. The results have group of multicellular larity. Similarly, dramatic advances in develop- demonstrated that several reasons typically as- δ-proteobacteria, also mental genetics and comparative genomics are sociated with transitions to multicellularity, known as significantly enriching our understanding of the such as predation avoidance or higher feeding myxomycetes, with a genetic changes associated with multicellular efficiency, do indeed confer a selective advan- complex life-cycle during which they transitions, and of the origins of the animal de- tage over unicellularity. For example, a number construct a velopmental program in particular. The body of algal species were able to evolve multicellu- multicellular fruiting of facts now emerging has shed ample light on larity when grown in culture in the presence body the tempo and pattern of this pivotal period in of predators, thus dramatically reducing their life’s history and is setting up the framework chances of being eaten (11, 47, 66). Similarly, within which we can understand the origins and Volvox algae (61) and myxobacteria (88) have assembly of the genetic toolkit for animal mul- been shown to be at advantage when multicel- ticellularity and development. lular because of their ability to better utilize available nutrients. Most manifestations of multicellularity are THE EVOLUTION OF relatively simple in architecture, involving MULTICELLULARITY: A only a very small number of cell types (19, 58) COMPARATIVE PERSPECTIVE (Table 1). Cell-type determination typically occurs via the action of a small number of regu- Why Did Multicellularity Evolve? latory proteins (49). However, the large number It is statistically unlikely that complex pheno- of regulatory proteins present in both prokary- types arise repeatedly by chance (25). Thus, otes and eukaryotes suggests that, from a ge- from a comparative perspective, the multiple nomic point of view, these organisms have the origins of multicellularity in a wide variety of potential to generate a much larger number of organisms from distinct evolutionary lineages cell types than those actually observed (19). So underscore the notion that key aspects of this why do most multicellular organisms possess so phenotype are likely to be, under certain con- few cell types? Although it is difficult to address ditions, selectively advantageous. Considerable this question a posteriori, a plausible explana- attention has been devoted to identifying what tion may be that there was no selective pressure these aspects or conditions may have been, with for early microscopic multicellular organisms a variety of factors implicated as plausible con- to further increase their size, and consequently tributors to multicellularity’s repeated inven- diversify their pool of cell types beyond a small Annu. Rev. Genet. 2008.42:235-251.
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